Oviposition of fruit flies (Diptera: Tephritidae) and its relation with the pericarp of citrus fruits - SciELO
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Brazilian Journal of Biology http://dx.doi.org/10.1590/1519-6984.167661
ISSN 1519-6984 (Print)
Original Article
ISSN 1678-4375 (Online)
Oviposition of fruit flies (Diptera: Tephritidae) and its relation
with the pericarp of citrus fruits
N. P. Diasa*, D. E. Navab, M. S. Garciaa, F. F. Silvac and R. A. Valgasb
a
Programa de Pós-graduação em Fitossanidade, Universidade Federal de Pelotas – UFPel,
Campus Universitário, s/n, CEP 96900-010, Capão do Leão, RS, Brazil
b
Laboratório de Entomologia, Empresa Brasileira de Pesquisa Agropecuária – Embrapa,
Rodovia BR-392, Km 78, CEP 96010-970, Pelotas, RS, Brazil
Laboratório de Entomologia, Universidade Federal do Pampa – UNIPAMPA,
c
Av. Luiz Joaquim de Sá Britto, s/n, CEP 97650-000, Itaqui, RS, Brazil
*e-mail: nayma.dias@gmail.com
Received: August 8, 2016 – Accepted: March 7, 2017 – Distributed: October 31, 2018
Abstract
Fruit flies (Diptera: Tephritidae) represent a threat to fruit growing worldwide, mainly the citrus culture, however,
biological studies show that fruit flies are not perfectly adapted to this host. This study investigated oviposition of
Anastrepha fraterculus (Wiedemann, 1830) and Ceratitis capitata (Wiedemann, 1824) and its relation with the pericarp
of citrus fruits. We evaluated the relationship between depth of oviposition of A. fraterculus and C. capitata and epicarp
thickness of orange [Citrus sinensis (L.) Osbeck)] ‘Navelina’ and tangerine [C. reticulata (L.)] ‘Clemenules’ and
the influence of fruit mesocarp of tangerine ‘Clemenules’ on oviposition of these species. The study was conducted
under controlled conditions of temperature (25 ± 2 °C), relative humidity (70 ± 10% RH) and photophase (12 h).
A. fraterculus and C. capitata laid their eggs in the flavedo region of orange ‘Navelina’ and between the albedo and
flavedo of tangerine ‘Clemenules’. When fruits with mesocarp exposed were offered, there was no oviposition by both
fruit fly species. The results show that epicarp thickness of citrus fruits did not influence oviposition of A. fraterculus
and C. capitata as oviposition did not occur only in the presence of the mesocarp, suggesting that other factors are
involved in oviposition of these species.
Keywords: Anastrepha fraterculus, Ceratitis capitata, citrus peel structure, epicarp, mesocarp.
Oviposição de moscas-das-frutas (Diptera: Tephritidae) e
sua relação com o pericarpo de frutos cítricos
Resumo
As moscas-das-frutas (Diptera: Tephritidae) representam um risco à fruticultura mundial, especialmente na cultura dos
citros, entretanto estudos biológicos demonstram que as moscas-das-frutas não estão perfeitamente adaptadas à estes
hospedeiros. Este estudo investigou a oviposição de Anastrepha fraterculus (Wiedemann, 1830) e Ceratitis capitata
(Wiedemann, 1824) e sua relação com o pericarpo de frutos cítricos. Foi avaliada a relação entre a profundidade de
oviposição de A. fraterculus e de C. capitata e a espessura do epicarpo dos frutos de laranjeira [Citrus sinensis (L.)
Osbeck)] ‘Navelina’ e tangerineira [C. reticulata (L.)] ‘Clemenules’ e a influência do mesocarpo de frutos de tangerineira
‘Clemenules’ na oviposição destas espécies. O estudo foi conduzido em condições controladas de temperatura (25 ± 2 °C),
umidade relativa (70 ± 10%) e fotofase (12 horas). A. fraterculus e C. capitata depositaram ovos no flavedo de frutos de
laranjeira ‘Navelina’ e entre o flavedo e o albedo de frutos de tangerineira ‘Clemenules’. Quando oferecido frutos com
mesocarpo exposto, não houve oviposição por ambas as espécies de mosca. Os resultados demonstram que a espessura
do epicarpo de frutos cítricos não influenciou a oviposição de A. fraterculus e de C. capitata, a qual não ocorreu na
presença apenas do mesocarpo, sugerindo que outros fatores estão envolvidos na oviposição por estas espécies.
Palavras-chave: Anastrepha fraterculus, Ceratitis capitata, estrutura da casca de citros, epicarpo, mesocarpo.
1. Introduction
Citrus hosts a large number of pests worldwide, Anastrepha fraterculus (Wiedemann, 1830) and the
and of these, Tephritidae fruit flies may represent major Mediterranean fruit fly, Ceratitis capitata (Wiedemann,
pests (Onah et al., 2015). The South American fruit fly, 1824) (Diptera: Tephritidae) are reported as the most
Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 443-448 443/448 443Dias, N.P. et al.
common fruit fly pests attacking citrus in Brazil (Silva et al., a side opening for maintenance. The adults were fed with
2006; Paiva and Parra, 2013). a solid diet composed of sugar, wheat germ and yeast at
The selection of oviposition site of fruit flies is ratio 3:1:1 in a plastic container (50 mL).
critical for survival and success of their offspring
2.2. Depth of oviposition and its relation to epicarp
(Díaz‑Fleischer et al., 2000). In the citrus culture,
while fruit flies are considered major pests and causing thickness
economic losses (Muthuthantri and Clarke, 2012), many Fruits of orange [Citrus sinensis (L. Osbeck)] ‘Navelina’
authors believe that fruit files are not perfectly adapted and tangerine ‘Clemenules’ (Rutaceae) were offered to
to development in citrus fruits (Salvatore et al., 2004). females of A. fraterculus and C. capitata. For control,
For Back and Pemberton (1915), this lower performance fruits of papaya ‘Solo Golden’ (Carica papaya L.)
could be related to resistance mechanisms of citrus (Caricaceae), mango ‘Tommy Atkins’ (Mangifera indica L.)
fruits, such as chemical components of glands in the (Anacardiaceae) and guava ‘Paluma’ (Psidium guajava L.)
flavedo (epicarp) and albedo (mesocarp) elasticity that (Myrtaceae) were offered because they are natural
could generate mechanical resistance and consequently hosts and used for lab rearing (Fernandes-da-Silva and
hinder embryonic and larval development. Other factors Zucoloto, 1993; Joachim-Bravo and Silva Neto, 2004;
that affect performance for oviposition in citrus fruits Aluja et al, 2014). All fruits used in the experiments
comprise the gum produced by varieties of grapefruit were ripe according to the outside color of the peel for
(C. aradise) (Macfad), lime [C. aurantifolia (Christmas) each cultivar (Malevski et al., 1977; Bron and Jacomino,
Swingle] and lemon [(C. limon) (L. Burm)] (Rutaceae) 2006; Cavalini et al., 2006; Lado et al., 2014).
and the hardening of tissues around the oviposition hole. The fruits were individually exposed in the bottom
Susceptibility of citrus to fruit flies varies according plastic cages (24 × 12 × 17 cm) with 10 females of 15 d
to the fly species, fruit maturity, fruit species and cultivar, of age for a period of 24 h. After the exposure period,
oviposition behavior of the insect and consistency of the the fruits were removed and cut into thin slices (10 mm)
fruit peel are factors possibly involved in this process perpendicular to the fruit surface using a scalpel. After,
(Greany et al., 1983). Females of fruit flies consider
they were analyzed under a stereoscopic microscope
qualitative and quantitative aspects of the citrus fruit
with 10 x magnification (Model Stemi SV 11, Zeiss,
composition in the selection process for an oviposition
Thornwood, NY) to identify the location of eggs in each
site. However, the exact location where females tend
fruit. The measurements were performed by determining
to lay their eggs in citrus fruits as well as the effects of
the distance (mm) of the front pole of the egg to the fruit
the physical characteristics of these fruits on oviposition
surface, as described by Perondini et al. (1998). Epicarp
remain unknown. Prokopy and Vargas (1996) believe
that epicarp thickness of citrus fruits could be an thickness (mm) of each fruit host was determined using
important criterion in infestation of fruit flies. Thus, the a digital caliper (Model Hardened, Shainless, China)
host range of tephritid fruit flies may be restricted by with 10 repetitions for each fruit specie. For citrus fruit,
the ability of the insect to penetrate the peel of the host besides epicarp (flavedo) thickness (mm), mesocarp
fruit (Rattanapun et al., 2009, 2010). Thus, this study (albedo) thickness was also measured and peel thickness
investigated oviposition of A. fraterculus and C. capitata consisted of the sum of the two measurements.
and its relation with the pericarp of citrus fruits. To express the insertion degree of the ovipositor
regarding fruit peel thickness, we used an index calculated
2. Material and Methods by , where: I = insertion index, that is, the number of
times the ovipositor exceeded peel thickness and laid
The study was conducted in Pelotas, Rio Grande egg (s); o = distance between the front pole of the egg
do Sul State, Brazil, under controlled conditions of to fruit surface (mm); e = peel thickness (mm). In this
temperature (25 ± 2 °C), relative humidity (70 ± 10% RH) index, when I is greater than 1 (I > 1), it was considered
and photophase (12 h). that the ovipositor surpassed the entire peel.
2.1. Maintenance rearing For both species of fruit fly, it was determined the
The population of A. fraterculus was reared in mango total aculeus length (mm) from samples of 10 females
(Mangifera indica L.) (Anacardiaceae) while C. capitata kept in alcohol 70°. For these measurements, the
was reared in papaya (Carica papaya L.) (Caricaceae). aculeus was extended, removed from the eversible
The fruits were exposed to the flies for oviposition for a membrane and analyzed in stereoscopic microscope
period of 24 h, when the fruits were removed and packed with 10 x magnification (Model Stemi SV 11, Zeiss,
in plastic containers (11 × 12 × 19 cm) covered with Thornwood, NY).
TNT fabric (non-woven fabric). The containers were The experiment was conducted in completely randomized
lined with a fine vermiculite texture and after pupation, design with five treatments (different fruit species) and
the insects were transferred to Petri dishes (10 × 1.5 cm) 10 repetitions (fruit). Data on oviposition depth and
containing moistened vermiculite where they remained peel thickness (mm) of each host fruit were submitted
until emergence. The adult insects were kept in wooden to the Pearson linear correlation (r) through resampling
cages (50 × 50 × 40 cm) lined with voile fabric and with (bootstrap) with 5000 simulations (BioEstat 5.3).
444 444/448 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 443-448Oviposition of fruit flies in citrus
2.3. Influence of mesocarp of tangerine fruit on lower than in mango. In citrus fruits, insertion indexes for
oviposition both orange and tangerine were the lowest among all hosts
Four substrates were offered to females of A. fraterculus evaluated (Table 1).
and C. capitata for oviposition. The substrates consisted For both fruit fly species, the ovipositor did not
of tangerines ‘Clemenules’: 1) whole fruit; 2) fruit without completely surpass the flavedo in orange (I < 1), but for
epicarp; 3) fruit without epicarp covered with Parafilm A. fraterculus, the ovipositor surpassed the flavedo (I > 1),
(Kasvi, Curitiba, Brazil); and 4) only epicarp cut into however, it did not exceed the albedo in tangerine (I < 1)
8 cm diameter circle × 0.32 cm thick. The substrates were reaching only 0.07 mm (oviposition depth minus flavedo
offered in plastic cages (24 × 12 × 17 cm) to 10 females thickness) (Table 2). Similar situation for C. capitata,
of 15 d of age for a period of 24 h. After exposure, the which reached only 0.08 mm of the albedo (Table 2).
substrates were removed and analyzed under a stereoscopic
3.2. Influence of fruit mesocarp of tangerine fruit on
microscope with 10 x magnification (Model Stemi SV 11,
oviposition
Zeiss, Thornwood, NY) to count the eggs.
The experiment was conducted in completely randomized Significant difference was observed for oviposition
design with four treatments (substrate type) and 10 repetitions among tangerine substrates for A. fraterculus (H = 25.18,
(substrate). The data on the average number of eggs in each gl = 3, p < 0.0001) and C. capitata (H = 23.97, gl = 3,
substrate were tested for normality by the Shapiro-Wilk p < 0.0001). The number of eggs of A. fraterculus and
test (p ≤ 0.05). The means were subjected to analysis of C. capitata differed significantly when different substrates
variance using the Kruskal-Wallis test (p ≤ 0.05) followed for oviposition were offered (Table 3). Oviposition occurred
by the Dunn test (p ≤ 0.05) (BioEstat 5.3). for A. fraterculus and C. capitata when the whole tangerine
fruit and fruit with epicarp exposed cut in a circle were
3. Results offered to the ovipositors, differing significantly from the
other treatments where oviposition did not occur.
3.1. Depth of oviposition and its relation to epicarp
thickness
4. Discussion
For A. fraterculus, there was no significant correlation
between the insertion depth and epicarp thickness in any Epicarp thickness of oranges ‘Navelina’ and tangerine
of the hosts (p > 0.05). C. capitata presented a significant ‘Clemenules’ did not influence oviposition of A. fraterculus
correlation and directly proportional in mango (p = 0.0328). and C. capitata. The insects laid eggs in the flavedo region
The largest number of eggs was obtained in mango of orange ‘Navelina’ and between the albedo and flavedo
for A. fraterculus and in papaya for C. capitata (Table 1). in tangerine ‘Clemenules’. These data corroborate the
The insertion index was higher in mango than in the other results obtained by Papachristos and Papadopoulos (2009).
hosts, that is, the ovipositor exceeded epicarp thickness more The authors found no correlation between fecundity of
than 16 times for C. capitata and 14 times for A. fraterculus C. capitata in citrus fruits and their physical characteristics
(Table 1). For papaya and guava, the insertion indexes were such as epicarp thickness.
Table 1. Number of eggs, oviposition depth (mm), peel thickness (mm), flavedo and albedo thickness (mm) (± SD) and
insertion index (I) in five fruits for Anastrepha fraterculus and Ceratitis capitata. Temperature 25 ± 2°C, 70 ± 10% RH and
photophase of 12 h.
Total number Oviposition Peel thickness Flavedo/Albedo thickness Insertion
Fruit speciea of eggs depth (mm) (mm) (mm)b index (I)c
Anastrepha fraterculus
Papaya 42±1.87 0.72±0.06 0.49±0.04 - 1.46
Mango 169±4.30 2.63±0.25 0.19±0.03 - 14.09
Guava 53±2.16 5.74±0.18 4.86±0.25 - 1.18
Orange 35±1.43 0.15±0.09 2.68±0.16 (0.60±0.10/2.08±0.17) 0.05
Tangerine 61±1.96 1.56±0.14 2.11±0.14 (1.49±0.10/0.62±0.09) 0.74
Ceratitis capitata
Papaya 178±4.02 1.35±0.10 0.49±0.04 - 2.74
Mango 60±0.81 3.06±0.19 0.19±0.03 - 16.36
Guava 43±1.25 5.57±0.13 4.86±0.25 - 1.15
Orange 57±1.25 0.26±0.39 2.68±0.16 (0.60±0.10/2.08±0.17) 0.10
Tangerine 55±1.84 1.57±0.15 2.11±0.14 (1.49±0.10/0.62±0.09) 0.74
a
Cultivars: papaya Solo ‘Golden’, mango ‘Tommy Atkins’, guava ‘Paluma’, orange ‘Navelina’ and tangerine ‘Clemenules’;
b
Segments of citrus peel; cInsertion index (I) obtained from the relationship between oviposition depth (mm) and peel thickness (mm).
Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 443-448 445/448 445Dias, N.P. et al.
Table 2. Insertion index (I) and average of aculeus length (± SD) of Anastrepha fraterculus and Ceratitis capitata in flavedo
(epicarp) and albedo (mesocarp) of citrus fruits. Temperature 25 ± 2 °C, 70 ± 10% RH and photophase of 12 h.
Insertion index (I) Aculeus length (mm)
Fruit
Anastrepha fraterculus 1.56±0.15
Flavedo Albedo -
Orange ‘Navelina’ 0.25 0.00 -
Tangerine ‘Clemenules’ 1.07 0.17 -
Ceratitis capitata 1.33±0.19
Flavedo Albedo -
Orange ‘Navelina’ 0.43 0.00 -
Tangerine ‘Clemenules’ 1.08 0.19 -
Table 3. Average number of eggs (± SD) of Anastrepha C. capitata, which also infests native fruits but prefers
fraterculus and Ceratitis capitata in tangerine ‘Clemenules’. mainly exotic hosts (Branco et al., 2000).
Temperature 25 ± 2 °C, 70 ± 10% RH and photophase The lower insertion index in orange compared to
of 12 h. other treatments may indicate that this host has increased
Number of eggs resistance to infestation of fruit flies even compared to
Substrate Anastrepha Ceratitis tangerine (Table 1). Papachristos and Papadopoulos (2009)
fraterculus capitata evaluated five citrus cultivars (orange ‘Newhall’, orange
Whole fruit 3.9 ±1.10a 2.6 ±1.34a ‘Merlin’, orange ‘Xino Artas’, tangerine ‘Arta’ and lemon
Fruit epicarp 0.0 ±0.00b 0.0 ±0.00b ‘Maglini’) and found that females of C. capitata failed to
Fruit without covered 0.0 ±0.00b 0.0 ±0.00b lay eggs inside the fruit.
epicarp The lower consistency of tangerine peel can also be
Epicarp cut in circles 1.1 ±1.10ab 2.3 ±1.25a considered a key factor in fruit susceptibility to the attack
Values followed by different letters in column differ by the of A. fraterculus. According to Branco et al. (2000),
Dunn test (p ≤ 0.05). in addition to reduction on essential oil contents, peel
firmness decreases allowing higher larval survival due to
lower difficulty of the larva to migrate from peel to pulp.
The larger number of eggs of A. fraterculus obtained
The results of this study corroborate the work performed
in mango and C. capitata from papaya may be related
by Greany et al. (1983) that found tangerines more
to “pre-imaginal conditioning”, since the insects used
susceptible to the attack of Anastrepha suspensa (Loew)
in the experiment were reared in this host. The highest
than orange and lemon.
insertion index obtained in mango may have occurred
The higher insertion index of C. capitata in orange,
due to the smaller peel thickness of these fruits (0.19 mm)
although did not exceed the flavedo region, may have
compared to other treatments, since there was no significant occurred due to the greater number of eggs, since the aculeus
correlation between peel thickness and the number of eggs length of this species is shorter than that of A. fraterculus
of C. capitata. (Tables 1 and 2). Branco et al. (2000) report that when
In papaya, the lower insertion index estimated for females lay several eggs in the same region of the fruit,
C. capitata compared to the indexes obtained for mango as it occurs for C. capitata, there may be a breakdown in
fruit can be related to the presence of benzyl isothiocyanate fruit resistance allowing at least part of the eggs to develop.
(BITC) in fruit. This substance is present at high The data obtained show that peel thickness of citrus
concentrations in unripe papaya fruit and decreases as the fruits does not influence oviposition depth of C. capitata
fruit ripens, suggesting that only ripe fruits are infested in and A. fraterculus and that other factors may be involved
the field, however, at a smaller number of A. fraterculus in this process. The flavedo constitution is cited by several
(Seo et al., 1983). This data indicates that C. capitata authors as the most critical resistance mechanism to fruit
can be less affected by BITC, corroborating the results flies infestation in citrus (Back and Pemberton, 1915;
presented by Joachim-Bravo and Silva Neto (2004) who Greany et al., 1983; Salvatore et al., 2004; Ioannou et al.,
reported preference for papaya fruit for oviposition of 2012). Possibly, when oil glands in the flavedo are broken,
C. capitata, followed by mango and orange, confirming they release toxic compounds that, in contact with eggs
the data obtained in this study (Table 1). and first instar larvae, can cause death before the larvae
In guava, the lowest index estimated for papaya and reach the albedo region (non-oily region of the peel)
mango fruits may be attributed to the influence of fruit (Greany, 1989).
chemical characteristics, such as pH and soluble solids C. capitata laid eggs at greater depth in orange and
(°Brix) as described by Branco et al. (2000). In these tangerine compared to A. fraterculus (Table 1). Back
fruits, the larger number of eggs of A. fraterculus may and Pemberton (1915) reported that when ovipositing at
have occurred due to its preference for native fruit, unlike greater depth, females ensure the survival of their offspring
446 446/448 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 443-448Oviposition of fruit flies in citrus
by not exposing the eggs to essential oil glands in the of immature stages of C. capitata, while limonene, found
flavedo. Greany et al. (1983) reported that egg viability in more than 90% in all citrus oils, stimulates oviposition
of A. suspensa laid between the oil glands in the flavedo justifying infestations of C. capitata in citrus fruits.
region was greater than that of eggs deposited directly Further studies are needed to evaluate the different
in the glands. hypotheses considered in this work. Studies on Tephritidae
Oil toxicity in the flavedo region for eggs and larvae of embryology and analyses of the oil glands in the flavedo
C. capitata can be attributed to the higher content of limonene region during oviposition as well as studies on comparative
in oranges (Papachristos et al., 2009). Salvatore et al. (2004) of toxicity of compounds that act on the oviposition behavior
evaluated egg viability of C. capitata laid in epicarp of four of these insects would help to answer these questions.
orange cultivars and found values between 19 and 49% of
viability. The same authors found that citral compounds, Acknowledgements
coumarin and linalool, extracted from lime ‘Sicilian’
caused mortality of larvae of C. capitata of up to 98%. The authors wish to thank National Counsel of Technological
The presence of chorion reticulation as well as and Scientific Development (CNPq), Coordination for the
respiratory appendages, common in fly eggs, could also Improvement of Higher Education Personnel (CAPES)
be an adaptation of these insects. Murillo and Jirón (1994) and the Brazilian Agricultural Research Corporation
found that A. obliqua showed greater oxygen demand by (EMBRAPA), for the financial support and scholarship.
depositing their eggs in a way that the respiratory appendages
remain outside of the fruit. However, Margaritis (1985)
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